Multiple functional roles of flavonoids in photoprotection

Abstract

Flavonoids have long been recognized as playing multiple roles in the responses of higher plants to a wide range of environmental constraints (Winkel-Shirley, 2002; Roberts & Paul, 2006), and early proposed as developmental regulators (Stafford, 1991). Over the last three decades, as ozone depletion has become a major environmental problem, the particular role of flavonoids in screening short-wavelength solar UV-B radiation (over the 280–315 nm waveband) has been strongly emphasized (Rozema et al., 1997; Burchard et al., 2000). It is now well documented that UV-B stress greatly enhances the production of reactive oxygen species (ROS), as occurs in response to a plethora of environmental stresses (Apel & Hirt, 2004; Jenkins, 2009). UV-B-responsive flavonoids in general have the potential to reduce the oxidative damage caused by short solar wavelengths, in addition to reducing the risk of ROS generation by attenuating the penetration of UV-B radiation to sensitive leaf targets (Kytridis & Manetas, 2006; Kotilainen et al., 2008; Owens et al., 2008; Agati et al., 2009). An increased ratio of the 'effective antioxidant' quercetin or luteolin glycosides to the 'poor antioxidant' kaempferol or apigenin glycosides has been reported for plants exposed to high levels of UV-B or sunlight irradiance (Markham et al., 1998; Ryan et al., 1998; Gerhardt et al., 2008; Agati et al., 2009). Flavonoids occur not only in the vacuoles and cell walls of epidermal cells and in nonsecretory and glandular trichomes (Wollenweber & Dietz, 1981; Strack et al., 1988; Hutzler et al., 1996; Tattini et al., 2007), but also in the vacuoles of mesophyll cells (Kytridis & Manetas, 2006; Agati et al., 2009) and in chloroplasts (Saunders & McClure, 1976; Takahama, 1982; Agati et al., 2007). As a consequence, they are optimally located to reduce light-induced oxidative damage near or within the sites of ROS production. Recently, a nuclear distribution of orthodihydroxylated B-ring flavonoids has been suggested to protect DNA from oxidative damage (Feucht et al., 2004). Flavonoids have been reported to modulate auxin movement (Peer & Murphy, 2007) and hence have the potential to regulate the development of plants growing under different intensities of sunlight irradiance (Jansen, 2002; Buer & Djordjevic, 2009). Antioxidant flavonoids are the most effective inhibitors of basipetal auxin transport (Jacobs & Rubery, 1988;Brown et al., 2001; Jansen et al., 2001). Strong similarities have been found in the molecular targets of flavonoid modulation of auxin movement and signaling components vital to animal cellular functions (Taylor & Grotewold, 2005). In both cases the ability of flavonoids to bind to the ATP sites of a large number of proteins (e.g. the auxin efflux facilitator PIN proteins in plants,Peer et al., 2004) has been invoked, this ability being restricted to flavonoid structures with potentially effective 'antioxidant' properties (Williams et al., 2004). Here, we offer evidence that may challenge the view that light-inducible 'UV-absorbing flavonoids' function primarily in attenuating short-wavelength solar UV-B radiation. We propose that UV-absorbing flavonoids serve an important antioxidant function in photoprotection. Our suggestion is based upon: the UV-screening and antioxidant properties of UV-inducible flavonoids; their accumulation in the mesophyll, not only in epidermal cells following sunlight exposure; the minor role of effective UV attenuators, such as hydroxycinnamic acid derivatives, in the response of plants to sunlight irradiance; and the high capacity of antioxidant flavonoid structures to regulate auxin movement. Most 'UV-absorbing flavonoids', with the exception of acylated structures, do not maximally absorb over the 280–315-nm waveband and hence do not equip the leaf with the most effective shield against UV-B irradiance, as compared with other phenylpropanoids (Harborne & Williams, 2000). Nevertheless, flavonoids accumulate to a greater extent than other phenylpropanoids in response to UV-B radiation. Most 'flavonoid anthocyanins' have negligible molar extinction coefficients (ε) over the 280–390-nm waveband, but increase greatly in concentration in response to UV irradiance (for review articles, see Gould, 2004; Manetas, 2006). The best candidates for UV-B attenuators are hydroxycinnamic acid derivatives (e.g. p-coumaric, ferulic and caffeic acid), with εmax in the 310–325-nm waveband (Harborne & Williams, 2000; Tattini et al., 2004). However, the ratio of flavonoids to hydroxycinnamates increases steeply upon exposure to UV-B or strong sunlight (Burchard et al., 2000; Tattini et al., 2000; Agati et al., 2002; Kotilainen et al., 2008). Flavonoids seem to 'replace' hydroxycinnamic acid derivatives as a leaf develops under UV irradiance (Burchard et al., 2000), and soluble hydroxycinnamates are usually confined to tissues receiving the lowest doses of UV radiation (Olsson et al., 1999; Tattini et al., 2004). Consequent